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Sympathetic and Baroreceptor Reflex Function in Neurally Mediated Syncope Evoked by Tilt

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Sympathetic and Baroreceptor Reflex Function in Neurally Mediated Syncope Evoked by Tilt Sympathetic and baroreceptor reflex function in neurally mediated syncope evoked by tilt. R Mosqueda-Garcia, … , R M Robertson, D Robertson J Clin Invest. 1997;99(11):2736-2744. https://doi.org/10.1172/JCI119463. Research Article The pathophysiology of neurally mediated syncope is poorly understood. It has been widely assumed that excessive sympathetic activation in a setting of left ventricular hypovolemia stimulates ventricular afferents that trigger hypotension and bradycardia. We tested this hypothesis by determining if excessive sympathetic activation precedes development of neurally mediated syncope, and if this correlates with alterations in baroreflex function. We studied the changes in intraarterial blood pressure (BP), heart rate (HR), central venous pressure (CVP), muscle sympathetic nerve activity (MSNA), and plasma catecholamines evoked by upright tilt in recurrent neurally mediated syncope patients (SYN, 5+/-1 episodes/mo, n = 14), age- and sex-matched controls (CON, n = 23), and in healthy subjects who consistently experienced syncope during tilt (FS+, n = 20). Baroreflex responses were evaluated from changes in HR, BP, and MSNA that were obtained after infusions of phenylephrine and sodium nitroprusside. Compared to CON, patients with SYN had blunted increases in MSNA at low tilt levels, followed by a progressive decrease and ultimately complete disappearance of MSNA with syncope. SYN patients also had attenuation of norepinephrine increases and lower baroreflex slope sensitivity, both during tilt and after pharmacologic testing. FS+ subjects had the largest decrease in CVP with tilt and had significant increases in MSNA and heart rate baroreflex slopes. These data challenge the view that excessive generalized sympathetic activation […] Find the latest version: https://jci.me/119463/pdf Sympathetic and Baroreceptor Reflex Function in Neurally Mediated Syncope Evoked by Tilt Rogelio Mosqueda-Garcia,*‡§ Raffaello Furlan,‡ Roxana Fernandez-Violante,‡ Tushar Desai,* Marie Snell,* Zoltan Jarai,* Vasu Ananthram,§ Rose Marie Robertson,*§ and David Robertson*‡§ *Syncope Service in the Autonomic Dysfunction Unit and ‡Division of Clinical Pharmacology, §Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee 37232-2195 Abstract bradycardia (1). In susceptible individuals, this syndrome evolves in response to relative circulating hypovolemia or dur- The pathophysiology of neurally mediated syncope is poorly ing emotional overstimulation (2). Syncope resembling that understood. It has been widely assumed that excessive sym- termed “neurally mediated syncope” can also be evoked in pathetic activation in a setting of left ventricular hypovo- otherwise healthy subjects during prolonged upright tilt (3, 4), lemia stimulates ventricular afferents that trigger hypotension infusion of vasodilator substances (5), or during pronounced and bradycardia. We tested this hypothesis by determining lower body negative pressure (6, 7). It has been assumed that if excessive sympathetic activation precedes development of patients who are prone to this type of syncope have baroreflex neurally mediated syncope, and if this correlates with alter- mechanisms and hemodynamic responses qualitatively similar ations in baroreflex function. We studied the changes in in- to those of healthy subjects and differ only quantitatively traarterial blood pressure (BP), heart rate (HR), central (8, 9). venous pressure (CVP), muscle sympathetic nerve activity Based on experimental observations in nonfainting normal (MSNA), and plasma catecholamines evoked by upright tilt volunteers, it has been proposed that an initial exaggerated in recurrent neurally mediated syncope patients (SYN, 5Ϯ1 sympathetic activation, in combination with relative ventricu- episodes/mo, n ϭ 14), age- and sex-matched controls (CON, lar hypovolemia, stimulates myocardial ventricular afferents. n ϭ 23), and in healthy subjects who consistently experi- Stimulation of these afferents may result in reflex vasodilation enced syncope during tilt (FSϩ, n ϭ 20). Baroreflex re- with or without bradycardia (10–12). Alternatively, others have sponses were evaluated from changes in HR, BP, and MSNA proposed that a sudden central resetting of baroreflexes pro- that were obtained after infusions of phenylephrine and so- duces loss of sympathetic vascular control with subsequent dium nitroprusside. Compared to CON, patients with SYN syncope (13). had blunted increases in MSNA at low tilt levels, followed Some studies have suggested that the vasodilatation seen in by a progressive decrease and ultimately complete disap- neurally mediated syncope results from a withdrawal of sym- pearance of MSNA with syncope. SYN patients also had at- pathetic tone (14–16). Consistent with this view, there is evi- tenuation of norepinephrine increases and lower baroreflex dence of reduced cardiac and renal norepinephrine (NorEpi)1 slope sensitivity, both during tilt and after pharmacologic spillover in patients who fainted during cardiac catheterization testing. FSϩ subjects had the largest decrease in CVP with (17). In addition, sympathetic withdrawal has been observed tilt and had significant increases in MSNA and heart rate using microneurography in healthy subjects undergoing infu- baroreflex slopes. These data challenge the view that exces- sion of vasodilator agents (2, 18) or during pronounced lower sive generalized sympathetic activation is the precursor of body negative pressure (6). There is only one report studying the hemodynamic abnormality underlying recurrent neu- sympathetic nerve traffic in a patient with a history of vasode- rally mediated syncope. (J. Clin. Invest. 1997. 99:2736–2744.) pressor attacks (19). In this report, disappearance of muscle Key words: neurocardiogenic syncope • vasovagal • micro- sympathetic nerve activity preceded a rather prolonged hy- neurography • tilt • baroreflex potensive attack, presumably triggered by emotional stress. To our knowledge, there are no studies in patients with Introduction recurrent neurally mediated syncope that characterize the changes in sympathetic nerve activity during the upright pos- Neurally mediated (vasovagal or neurocardiogenic) syncope ture, the position in which syncope typically occurs (2). Simi- results from excessive arteriolar dilatation and inappropriate larly, there is no information that correlates temporal changes in sympathetic nerve activity and NorEpi levels with the devel- opment of syncope or with changes in central venous pressure. Part of these results were presented in abstract form at the American There is also very little systematic information regarding po- Heart Association Annual Scientific Sessions in Atlanta, GA, 8–11 tential changes in baroreflex function in these patients. In the November, 1993 (1993. Circulation [Suppl.]. 88:I-84). present studies, in addition to evaluating sympathetic outflow Address correspondence to Dr. Rogelio Mosqueda-Garcia, Clini- during upright tilt, we studied reflex cardiovascular function in cal Research Center, MCN, Vanderbilt University Medical Center, normotensive controls, patients with a medical history of neu- Nashville, TN 37232-2195. Phone: 615-936-1750; FAX: 615-936-1906; rally mediated syncope, and healthy subjects who experienced E-mail: [email protected] syncope only during tilt. Received for publication 12 September 1996 and accepted in re- vised form 13 March 1997. J. Clin. Invest. 1. Abbreviations used in this paper: CVP, central venous pressure; © The American Society for Clinical Investigation, Inc. Epi, epinephrine; FSϩ, subjects with false-positive tilt; HR, heart 0021-9738/97/06/2736/09 $2.00 rate; MSNA, muscle sympathetic nerve activity; NorEpi, norepineph- Volume 99, Number 11, June 1997, 2736–2744 rine; SYN, patients with recurrent syncope. 2736 Mosqueda-Garcia et al. Methods fossa. In the opposite arm, an intravenous line was positioned for blood sampling or drug administration. Study groups and patient selection. The subjects abstained from caf- Muscle sympathetic nerve activity (MSNA) was recorded from feine-containing products and smoking for at least 7 d. All medica- the right peroneal nerve using the microneurography technique (20, tions were stopped for at least five drug half-lives before the study. 21) described elsewhere (22, 23). In brief, the right leg was immobi- The first group of patients included 14 subjects (5 males and 9 fe- lized and securely positioned on the tilt table using an adjustable leg males, age range ϭ 21–41 yr, mean ϭ 34Ϯ1.32 yr) suffering from re- brace to maximize successful recordings. A unipolar tungsten elec- current syncope (SYN, two or more episodes per month) who were trode (uninsulated tip diameter of 1–5 ␮m, shaft diameter of 200 ␮m) recruited from the Vanderbilt Autonomic Dysfunction Center. In this was inserted into the muscle nerve fascicles of the peroneal nerve for group, the diagnosis was established after a review of the patient’s multiunit recordings. Nerve activity was fed to a preamplifier (1,000- medical history, a comprehensive physical examination, and a tilt ta- fold amplification) and filtered using a bandwidth between 700 and -fold, and in-100 ف ble study that indicated the presence of this syndrome. In addition, 2,000 Hz. The signal was then rectified, amplified these patients had negative cardiologic (12-lead EKG, echocardio- tegrated (time constant ϭ 0.1 s) to obtain a mean voltage display of gram, and ambulatory electrocardiographic monitoring), neurologic
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